Lutar, esconder ou correr: como Tamandua tetradactyla (Mammalia) em cativeiro responde a pistas indiretas de um predador?
DOI:
https://doi.org/10.29215/pecen.v5i0.1689Resumo
No ambiente natural, os animais são expostos a uma grande quantidade de ameaças a sobrevivência. Considerar a ecologia do medo é importante para estimar o papel ecossistêmico que os predadores desempenham nas comunidades, uma vez que o medo de um predador pode provocar não somente respostas baseadas em densidade (i.e., remoção de indivíduos de uma população), como também respostas comportamentais, que podem resultar em efeitos em cascata. Comportamentos defensivos são relativamente simples de serem avaliados em situação de cativeiro, uma vez que são conspícuos e específicos, dificilmente sendo confundidos com outros comportamentos quando observados. Desta forma, o objetivo deste estudo foi verificar a habilidade de indivíduos de Tamandua tetradactyla (Linnaeus, 1758) em detectar pistas indiretas de um predador, para avaliação de risco do ambiente. Neste estudo, seis indivíduos de tamanduás-mirim (T. tetradactyla) em cativeiro foram expostos a pistas indiretas (e.g., urina e fezes) de jaguatirica (Leopardus pardalis). No total, cinco machos e uma fêmea de tamanduá foram observados pelo método de animal focal, em um esforço total de 36 horas de observação. Tamanduás-mirins alocados nos recintos com pistas indiretas do predador exibiram maior frequência de comportamentos anti-predatórios e diminuição dos comportamentos de inatividade. A utilização de pistas indiretas é vantajosa para indivíduos de tamanduá-mirim, pois permitem a avaliação de risco de uma determinada mancha do ambiente e elicia comportamentos de evitação, que são menos custosos energeticamente. A porcentagem de comportamentos também é apresentada com e sem as pistas indiretas do predador de T. tetradactyla, na qual pode ser útil para entender a capacidade de resposta de tamanduás-mirins a situações de perigo.
Palavras chave: Ecologia do medo, tamanduá-mirim, jaguatirica, comportamentos anti-predatórios.
Referências
Altmann J. (1974) Observational study of Behaviour: sampling methods. Behaviour, 49: 227–266. https://doi.org/10.1163/156853974X00534
Amo L., Visser M.E. & Van Oers K. (2011) Smelling out predators is innate in birds. Ardea, 99: 177–184. https://doi.org/10.5253/078.099.0207
Banks P.B. (1998) Responses of Australian bush rats, Rattus fuscipes, to the odor of introduced Vulpes vulpes. Journal of Mammalogy, 79: 1260–1264. https://doi.org/10.2307/1383017
Bates D., Mächler M., Bolker B. & Walker S. (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv: 1406.5823.
Bianchi R.D.C., Campos R.C., Xavier-Filho N.L., Olifiers N., Gompper M.E. & Mourão G. (2014) Intraspecific, interspecific, and seasonal differences in the diet of three mid-sized carnivores in a large neotropical wetland. Acta Theriologica, 59: 13–23. https://doi.org/10.1007/s13364-013-0137-x
Blake J.G., Mosquera D., Loiselle B.A., Swing K., Guerra J. & Romo D. (2012) Temporal activity patterns of terrestrial mammals in lowland rainforest of eastern Ecuador. Ecotropica, 18: 137–146.
Blanchard R.J. & Blanchard D.C. (1989) Antipredator defensive behaviors in a visible burrow system. Journal of Comparative Psychology, 103: 70–82. https://doi:10.1037/0735-7036.103.1.70
Caro S.P. & Balthazart J. (2010) Pheromones in birds: myth or reality? Journal of Comparative Psychology A, 196: 751–766. https://doi.org/10.1007/s00359-010-0534-4
Catapani M.L., Pires J.S.R. & Vasconcellos A.D.S. (2019) Single-or Pair-Housed: Which Is Better for Captive Southern Tamanduas? Journal of Applied Animal Welfare Science, 22: 289–297. https://doi.org/10.1080/10888705.2018.1508352
Chivers D.P. & Smith R.J.F. (1994) Fathead minnows, Pimephales promelas, acquire predator recognition whe alarm substance is associated with the sight of unfamiliar fish. Animal Behaviour, 48: 597–605. https://doi.org/10.1006/anbe.1994.1279
Dickman C.R. & Doncaster C.P. (1984) Responses of small mammals to red fox (Vulpes vulpes) odour. Journal of Zoology, 204: 521–531. https://doi.org/10.1111/j.1469-7998.1984.tb02384.x
Eguizábal G.V., Palme R.M., Superina C.J., Asencio M.C., García C. & Busso J.M. (2019) Characterization and correlations of Behavioural and adrenocortical activities of zoo‐housed lesser anteaters (Tamandua tetradactyla). Zoo Biology, 38: 334–342.
https://doi.org/10.1002/zoo.21492
Eiten G. (1978) Delimitation of the cerrado concept. Vegetatio, 36: 169–178.
https://doi.org/10.1007/BF02342599
El Balaa R. & Blouin‐Demers G. (2011) Anti‐predatory behaviour of wild‐caught vs captive‐bred freshwater angelfish, Pterophyllum scalare. Journal of Applied Ichthyology, 27: 1052–1056.
https://doi.org/10.1111/j.1439-0426.2011.01740.x
Fendt M. (2006) Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. Journal of Chemical Ecology, 32: 2617–2627.
https://doi: 10.1007/s10886-006-9186-9
Ferreira Neto G.D.S., Baccaro F.B., Spironello W.R., Benchimol M., Fleischer K., Quesada C.A., Sousa Gonçalves A.L., Pequeno P.A.L. & Barnett A.P.A. (2021) Soil fertility and anthropogenic disturbances drive mammal species richness and assemblage composition on tropical fluvial islands. Austral Ecology. https://doi:10.1111/aec.13023
Ferrero D.M., Lemon J.K., Fluegge D., Pashkovski S.L., Korzan W.J., Datta S.R., Spehr M., Fendt M. & Liberles S.D. (2011) Detection and avoidance of a carnivore odor by prey. Proceedings of the National Academy of Sciences, 108: 11235–11240. https://doi.org/10.1073/pnas.1103317108
Foster V.C., Sarmento P., Sollmann R., Tôrres N., Jácomo A.T., Negrões N. & Silveira L. (2013) Jaguar and puma activity patterns and predator‐prey interactions in four Brazilian biomes. Biotropica, 45: 373–379. https://doi.org/10.1111/btp.12021
Hegab I.M., Kong S., Yang S., Mohamaden W.I. & Wei W. (2015) The ethological relevance of predator odors to induce changes in prey species. Acta Ethologica, 18: 1–9.
https://doi.org/10.1007/s10211-014-0187-3
Hill A.M. & Lodge D.M. (1994) Diel changes in resource demand: competition and predation in species replacement among crayfishes. Ecology, 75: 2118–2126.
https://doi.org/10.2307/1941615
Korpimaki E., Koivunen V. & Hakkarainen H. (1996) Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation? Behavioral Ecology, 7: 30–34.
https://doi.org/10.1093/beheco/7.1.30
Lima S.L. (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience, 48: 25–34. https://doi.org/10.2307/1313225
Mathews F., Orros M., McLaren G., Gelling M. & Foster R. (2005) Keeping fit on the ark: assessing the suitability of captive-bred animals for release. Biological Conservation, 121: 569–577. https://doi.org/10.1016/j.biocon.2004.06.007
McLean I.G. (1997) Conservation and the ontogeny of behaviour (p. 132–156). In: Clemmons J.R. & Buchholz R. (Eds). Behavioral Approaches to Conservation in the Wild. Cambridge: Cambridge University Press. 404 p.
Medri I.M., Mourão G.M. & Rodrigues F.H. (2006) Mamíferos do Brasil. Londrina: Universidade Estadual de Londrina. 437 p.
Monclús R., Palomares F., Tablado Z., Martinez-Fonturbel A. & Palme R. (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia, 158: 615–623. https://doi.org/10.1007/s00442-008-1201-0
Montgomery G.G. (1985) Movements, foraging and food habits of the four extant species of neotropical vermilinguas (Mammalia: Myrmecophagidae) (p. 365–377). In: Montgomery G.G. (Ed.). The Evolution and Ecology of Armadillos, Sloths and Vermilinguas. Washington, DC.: Smithsonian Institution Press. 451 p.
Montgomery G.G. & Lubin Y.D. (1977) Prey influences on movements of Neotropical anteaters. In: Proceedings of the 1975 predator symposium. Missoula: Montana Forest and Conservation Experiment Station, University of Montana.
Navarro-Castilla Á. & Barja I. (2014) Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)? Behavioral Ecology and Sociobiology, 68: 1505–1512.
https://doi.org/10.1007/s00265-014-1759-y
Neto G.S.F., Barros A.C., Sobroza T.V., Neves P.U.C., Phillips M.J. & Guimarães E.F. (2020) Period of the day and food-based enrichment affect behaviour activity of Tamandua tetradactyla in captivity? Pesquisa e Ensino em Ciências Exatas e da Natureza, 4: e1498.
http://dx.doi.org/10.29215/pecen.v4i0.1498
Nomura F., Prado D., Silva V.H.M., Borges F.R., Dias R.E. & Rossa‐Feres D.D.C. (2011) Are you experienced? Predator type and predator experience trade‐offs in relation to tadpole mortality rates. Journal of Zoology, 284: 144–150.
https://doi.org/10.1111/j.1469-7998.2011.00791.x
Nowak RM. & Paradiso J. L. (1983) Walker’s mammals of the world. 4° edition. Baltimore and London: The Johns Hopkings Press. 1470 p.
Osada K., Miyazono S. & Kashiwayanagi M. (2014) Pyrazine analogs are active components of wolf urine that induce avoidance and fear-related behaviors in deer. Frontiers in Behavioral Neuroscience, 8: 276. https://doi.org/10.3389/fnbeh.2014.00276
Pardo Vargas L.E. (2018) Diversity and habitat use of medium-large sized mammals across oil palm landscapes in the Llanos region of Colombia. Thesis, College of Science and Engineering, James Cook University, Queensland, Australia.
https://doi.org/10.25903/5be8adb35232e
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Redford K.H. (1984) Mammalian myrmecophagy: feeding, foraging and food preference. Ph.D. dissertation, Harvard University, Cambridge, MA. 299 p.
Redford K.H. (1994) The edentates of the Cerrado. Edentata, 1: 4–10.
Ripple W.J. & Beschta R.L. (2012) Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction. Biological Conservation, 145: 205–213.
https://doi.org/10.1016/j.biocon.2011.11.005
Rodrigues F.H., Marinho-Filho J. & Dos Santos H.G. (2001) Home ranges of translocated lesser anteaters Tamandua tetradactyla in the cerrado of Brazil. Oryx, 35: 166–169.
https://doi.org/10.1046/j.1365-3008.2001.00162.x
Sih A., Kats L.B. & Moore R.D. (1992) Effects of predatory sunfish on the density, drift, and refuge use of stream salamander larvae. Ecology, 73: 1418–1430.
https://doi.org/10.2307/1940687
St-Cyr S., Abuaish S., Spinieli R.L. & McGowan P.O. (2018) Maternal predator odor exposure in mice programs adult offspring social behavior and increases stress-induced behaviors in semi-naturalistic and commonly-used laboratory tasks. Frontiers in Behavioral Neuroscience, 12: 136. https://doi.org/10.3389/fnbeh.2018.00136
Trovati R.G & Brito B.D. (2009) Nota sobre deslocamento e área de uso de tamanduá-mirim (Tamandua tetradactyla) translocado no Cerrado brasileiro. Neotropical Biology and Conservation, 4: 144–149. http://dx.doi.org/10.4013/nbc.2009.43.04
Ullah I., Zuberi A., Khan K.U., Ahmad S., Thörnqvist P.O. & Winberg S. (2017) Effects of enrichment on the development of behaviour in an endangered fish mahseer (Tor putitora). Applied Animal Behaviour Science, 186: 93–100.
https://doi.org/186:93-100. 10.1016/j.applanim.2016.10.016
Wernecke K.E.A., Vincenz D., Storsberg S., D’Hanis W., Goldschmidt J. & Fendt M. (2015) Fox urine exposure induces avoidance behavior in rats and activates the amygdalar olfactory cortex. Behavioural Brain Research, 279: 76–81. https://doi.org/10.1016/j.bbr.2014.11.020
Whitwell S.M., Amiot C., Mclean I.G., Lovegrove T.G., Armstrong D.P., Brunton D.H. & Ji W. (2012) Losing anti‐predatory behaviour: A cost of translocation. Austral Ecology, 37: 413–418.
https://doi.org/10.1111/j.1442-9993.2011.02293.x
Winter B. (2013) Linear models and linear mixed effects models in R: Tutorial 11. arXiv preprint arXiv:1308.5499.
Yin B., Gu C., Lu Y., Hegab I.M., Yang S., Wang A. & Wei W. (2017) Repeated exposure to cat urine induces complex behavioral, hormonal, and c-fos mRNA responses in Norway rats (Rattus norvegicus). The Science of Nature, 104: 1–8. https://doi.org/10.1007/s00114-017-1484-2
Ylönen H., Kortet R., Myntti J. & Vainikka A. (2007) Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm? Acta Oecologica, 31: 1–7.
https://doi.org/10.1016/j.actao.2005.05.007
Zanette L.Y & Clinchy M. (2019) Ecology of fear. Current Biology, 29: 309–313.
https://doi.org/10.1016/j.cub.2019.02.042
Zimbres B., Furtado M.M., Jácomo A.T.A., Silveira L., Sollmann R., Tôrres N.M., Machado R.B. & Marinho-Filho J. (2013) The impact of habitat fragmentation on the ecology of xenarthrans (Mammalia) in the Brazilian Cerrado. Landscape Ecology, 28: 259–269.
https://doi.org/10.1007/s10980-012-9832-2
Zuur A.F., Ieno E.N., Walker N., Saveliev A.A. & Smith G.M. (2009) Mixed effects models and extensions in ecology with R. Statistics for Biology and Health. New York: Springer-Verlag. 574 p. https://doi.org/10.1007/978-0-387-87458-6B
Downloads
Publicado
Edição
Secção
Licença
Autores que publicam nesta revista concordam com os seguintes termos / Authors who publish in this journal agree to the following terms:
A) Autor(es) e o periódico mantêm os direitos da publicação; os autores concedem ao periódico o direito de primeira publicação, sendo vedada sua reprodução total ou parcial sob qualquer caráter de ineditismo; qualquer utilização subsequente de trechos de manuscritos (e.g., figuras, tabelas, gráficos etc.) publicados na Pesquisa e Ensino em Ciências Exatas e da Natureza deve reconhecer a autoria e publicação original / Author (s) and the journal maintain the rights of publication; the authors grant the journal the right of first publication, being prohibited their total or partial reproduction in any character of novelty; any subsequent use of excerpts from manuscripts (e.g., figures, tables, graphics, etc.) published in Research and Teaching in Exact and Natural Sciences must acknowledge the original authorship and publication.
B) Autores tem o direito de disseminar a própria publicação, podendo, inclusive disponibilizar o PDF final do trabalho em qualquer site institucional ou particular, bem como depositar a impressão da publicação em bibliotecas nacionais e internacionais / Authors have the right to disseminate the publication itself, and may also make available the final PDF of the work in any institutional or private site, as well as depositing the printing of the publication in national and international libraries.
